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[1]E Boyden, F Zhang, E Bamberg, G Nagel and K Deisseroth: Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8, 1263-1268 (2005)
[2]F Zhang, L Wang, M Brauner, J Liewald, K Kay, N Watzke, P Wood, E Bamberg, G Nagel, A Gottschalk and K Deisseroth: Multimodal fast optical interrogation of neural circuitry. Nature 446, 633-639 (2007)
[3]V Gradinaru, M Mogri, K Thompson, J Henderson and K Deisseroth: Optical deconstruction of parkinsonian neural circuitry. Science 324, 354-359 (2009)
[4]F Zhang, V Gradinaru, A Adamantidis, R Durand, R Airan, L de Lecea and K Deisseroth: Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat Protoc 5, 439-456 (2010)
[5]J Robishaw and C Berlot: Translating G protein subunit diversity into functinoal specificity. Curr Opin Cell Biol 16, 206-209 (2004)
[6]T Cabrera-Vera, J Vanhauwe, T Thomas, M Medkova, A Preininger, M Mazzoni and H Hamm: Insights into G protein structure, function, and regulation. Endocr Rev 24, 765-781 (2003)
[7]U Gerber, C Gee and P Benquet: Metabotropic glutamate receptors: intracellular signaling pathways. Curr Opin Pharmacol 7, 56-61 (2007)
[8]P Lian, L Xu, C Geng, Y Qian, W Li, X Zhen and W Fu: A computational perspective on drug discovery and signal transduction mechanism of dopamine and serotonin receptors in the treatment of schizophrenia. Curr Pharm Biotechnol 15, 916-926 (2014)
[9]M van Wyk, J Pielecka-Fortuna, S Löwel and S Kleinlogel: Restoring the ON-switch in blind retinas: Opto-mGluR6, a next-generation, cell-tailored optogenetic tool. PLoS Biol 13, e1002143 (2015)
[10]J Levitz, C Pantoja, B Gaub, H Janovjak, A Reiner, A Hoagland, D Schoppik, B Kane, P Stawski, A Schier, D Trauner and EY Isacoff: Optical control of metabotropic glutamate receptors. Nat Neurosci 16, 507-516 (2013)
[11]R Airan, K Thompson, L Fenno, H Bernstein and K Deisseroth: Temporally precise in vivo control of intracellular signalling. Nature 458, 1025-1029 (2009)
[12]T Bjarnadóttir, D Gloriam, S Hellstrand, H Kristiansson, R Fredriksson and H Schiöth: Comprehensive repertoire and phylogenetic analysis of the G protein-coupled receptors in human and mouse. Genomics 88, 263-273 (2006)
[13]H Schiöth and R Frederiksson: The GRAFS classification system of G-protein coupled receptors in comparative perspective. Gen Comp Endocrinol 142, 94-101 (2005)
[14]H Choe, Y Kim, J Park, T Morizumi, E Pai, N Krauss, K Hofmann, P Scheerer and O Ernst: Crystal structure of metarhodopsin II. Nature 471, 651-655 (2011)
[15]A Doré, K Okrasa, J Patel, M Serrano-Vega, K Bennett, R Cooke, J Errey, A Jazayeri, S Khan, B Tehan, M Weir, G Wiggin and F Marshall: Structure of class C GPCR metabotropic glutamate receptor 5 transmembrane domain. Nature, 511, 557-562 (2014)
[16]K Hollenstein, J Kean, A Bortolato, R Cheng, A Doré, A Jazayeri, R Cooke, M Weir and F Marshall: Structure of class B GPCR corticotropin-releasing factor receptor 1. Nature 499, 438-443 (2013)
[17]S Rasmussen, B DeVree, Y Zou, A Kruse, K Chung, T Kobilka, F Thian P Chae, E Pardon, D Calinski, J Mathiesen, S Shah, J Lyons, M Caffrey, S Gellman, J Steyaert, G Skiniotis, W Weis, R Sunahara and B Kobilka: Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477, 549-555 (2011)
[18]T Schwartz, T Frimurer, B Holst, M Rosenkilde and C Elling: Molecular mechanism of 7TM receptor activation - a global toggle switch model. Annu Rev Pharmacol Toxicol 46, 481-519 (2006)
[19]J Pin, T Galvez and L Prézeau: Evolution, structure and activation mechanism of family 3/C G-protein-coupled receptors. Pharmacol Ther 98, 325-354 (2003)
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[24]D Gutierrez, M Mark, O Masseck, T Maejima, D Kuckelsberg, R Hyde, M Krause, W Kruse and S Herlitze: Optogenetic control of motor coordination by Gi/o protein-coupled vertebrate rhodopsin in cerebellar Purkinje cells. J Biol Chem 286, 25848-25858 (2011)
[25]J Kim, J Hwa, P Garriga, P Reeves, U RajBhandary and H Khorana: Light-driven activation of beta 2-adrenergic receptor signaling by a chimeric rhodopsin containing the beta 2-adrenergic receptor cytoplasmic loops. Biochemistry 44, 2284-2292 (2005)
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[33]I Tochitsky, A Polosukhina, V Degtyar, N Gallerani, C Smith, A Friedman, R Van Gelder, D Trauner, D Kaufer and R Kramer: Restoring visual function to blind mice with a photoswitch that exploits electrophysiological remodeling of retinal ganglion cells. Neuron 81, 800-813 (2014)
[34]K Yau and R Hardie: Phototransduction motifs and variations. Cell 139, 246-264 (2009)
[35]B Gaub, M Berry, A Holt, E Isacoff and J Flannery: Optogenetic vision restoration using rhodopsin for enhanced sensitivity. Mol Ther (2015), Epub ahead of print
[36]Y Shichida and T Matsuyama: Evolution of opsins and phototransduction. Philos Trans R Soc B 364, 2881-2895 (2009)
[37]H Bailes, L Zhuang and R Lucas: Reproducible and sustained regulation of Gαs signalling using a metazoan opsin as an optogenetic tool. PLoS One, 7, e30774 (2012)
[38]O Masseck, K Spoida, D Dalkara, T Maejima, JM Rubelowski, L Wallhorn, E Deneris and S Herlitze: Vertebrate cone opsins enable sustained and highly sensitive rapid control of Gi/o signaling in anxiety circuitry. Neuron 81, 1263-1273 (2014)
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[41]B Lin, A Koizumi, N Tanaka, S Panda and R Masland: Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc Natl Acad Sci U S A 105, 16009-16014 (2008)
[42]Z Melyan, E Tarttelin, J Bellingham, R Lucas and M Hankins: Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433, 741-745 (2005)
[43]T Tsunematsu, K Tanaka, A Yamanaka and A Koizumi: Ectopic expression of melanopsin in orexin/hypocretin neurons enables control of wakefulness of mice in vivo by blue light. Neurosci Res 75, 23-28 (2013)
[44]J Nissilä, S Mänttäri, T Särkioja, H Tuominen, T Takala, M Timonen and S Saarela: Encephalopsin (OPN3) protein abundance in the adult mouse brain. J Comp Physiol A 198, 833-839 (2012)
[45]D Kojima, S Mori, M Torii, A Wada, R Morishita and Y Fukada: UV-sensitive photoreceptor protein OPN5 in humans and mice. PLoS One 6, e26388 (2011)
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[50]B Kobilka, T Kobilka, K Daniel, J Regan, M Caron and R Lefkowitz: Chimeric alpha 2-, beta 2-adrenergic receptors: delineation of domains involved in effector coupling and ligand binding specificity. Science 240, 1310-1316 (1988)
[51]M Olah: Identification of A2a adenosine receptor domains involved in selective coupling to Gs. Analysis of chimeric A1/A2a adenosine receptors. J Biol Chem 272, 337-344 (1997)
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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
1 Institute for Physiology, University of Bern, Switzerland
Abstract
Optogenetics has taken biomedical research by storm. The power and precision at which light-gated ion channels control cellular excitability in diverse biological systems has convinced researchers of an optical future. Growing interest in optical methods has sparked the development of multiple new optogenetic tools, which allow precise control of numerous cellular processes. Among these new tools are the light-activatable G-protein coupled receptors (GPCRs) or Opto-GPCRs. The extent of the GPCR family, which in humans alone encompasses approximately 800 different proteins, and the immense therapeutic potential of Opto-GPCRs predict a big future for this juvenile field. Here the different approaches taken to design Opto-GPCRs are reviewed, outlining the advantages and disadvantages of each method for physiological and potential clinical application.
Keywords
- G-Protein Coupled Receptors
- Optogenetics
- Protein Engineering
- Opsin
- Signal Transduction
- G-Protein Specificity
- Designer Optogenetic Tools
- Chimeric G-Protein Coupled Receptors
- Review
References
- [1] E Boyden, F Zhang, E Bamberg, G Nagel and K Deisseroth: Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8, 1263-1268 (2005)
- [2] F Zhang, L Wang, M Brauner, J Liewald, K Kay, N Watzke, P Wood, E Bamberg, G Nagel, A Gottschalk and K Deisseroth: Multimodal fast optical interrogation of neural circuitry. Nature 446, 633-639 (2007)
- [3] V Gradinaru, M Mogri, K Thompson, J Henderson and K Deisseroth: Optical deconstruction of parkinsonian neural circuitry. Science 324, 354-359 (2009)
- [4] F Zhang, V Gradinaru, A Adamantidis, R Durand, R Airan, L de Lecea and K Deisseroth: Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat Protoc 5, 439-456 (2010)
- [5] J Robishaw and C Berlot: Translating G protein subunit diversity into functinoal specificity. Curr Opin Cell Biol 16, 206-209 (2004)
- [6] T Cabrera-Vera, J Vanhauwe, T Thomas, M Medkova, A Preininger, M Mazzoni and H Hamm: Insights into G protein structure, function, and regulation. Endocr Rev 24, 765-781 (2003)
- [7] U Gerber, C Gee and P Benquet: Metabotropic glutamate receptors: intracellular signaling pathways. Curr Opin Pharmacol 7, 56-61 (2007)
- [8] P Lian, L Xu, C Geng, Y Qian, W Li, X Zhen and W Fu: A computational perspective on drug discovery and signal transduction mechanism of dopamine and serotonin receptors in the treatment of schizophrenia. Curr Pharm Biotechnol 15, 916-926 (2014)
- [9] M van Wyk, J Pielecka-Fortuna, S Löwel and S Kleinlogel: Restoring the ON-switch in blind retinas: Opto-mGluR6, a next-generation, cell-tailored optogenetic tool. PLoS Biol 13, e1002143 (2015)
- [10] J Levitz, C Pantoja, B Gaub, H Janovjak, A Reiner, A Hoagland, D Schoppik, B Kane, P Stawski, A Schier, D Trauner and EY Isacoff: Optical control of metabotropic glutamate receptors. Nat Neurosci 16, 507-516 (2013)
- [11] R Airan, K Thompson, L Fenno, H Bernstein and K Deisseroth: Temporally precise in vivo control of intracellular signalling. Nature 458, 1025-1029 (2009)
- [12] T Bjarnadóttir, D Gloriam, S Hellstrand, H Kristiansson, R Fredriksson and H Schiöth: Comprehensive repertoire and phylogenetic analysis of the G protein-coupled receptors in human and mouse. Genomics 88, 263-273 (2006)
- [13] H Schiöth and R Frederiksson: The GRAFS classification system of G-protein coupled receptors in comparative perspective. Gen Comp Endocrinol 142, 94-101 (2005)
- [14] H Choe, Y Kim, J Park, T Morizumi, E Pai, N Krauss, K Hofmann, P Scheerer and O Ernst: Crystal structure of metarhodopsin II. Nature 471, 651-655 (2011)
- [15] A Doré, K Okrasa, J Patel, M Serrano-Vega, K Bennett, R Cooke, J Errey, A Jazayeri, S Khan, B Tehan, M Weir, G Wiggin and F Marshall: Structure of class C GPCR metabotropic glutamate receptor 5 transmembrane domain. Nature, 511, 557-562 (2014)
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- [21] T Yamashita, A Terakita and Y Shichida: The second cytoplasmic loop of metabotropic glutamate receptor functions at the third loop position of rhodopsin. J Biochem 130, 149-155 (2001)
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- [24] D Gutierrez, M Mark, O Masseck, T Maejima, D Kuckelsberg, R Hyde, M Krause, W Kruse and S Herlitze: Optogenetic control of motor coordination by Gi/o protein-coupled vertebrate rhodopsin in cerebellar Purkinje cells. J Biol Chem 286, 25848-25858 (2011)
- [25] J Kim, J Hwa, P Garriga, P Reeves, U RajBhandary and H Khorana: Light-driven activation of beta 2-adrenergic receptor signaling by a chimeric rhodopsin containing the beta 2-adrenergic receptor cytoplasmic loops. Biochemistry 44, 2284-2292 (2005)
- [26] M Banghart, K Borges, E Isacoff, D Trauner and R Kramer: Light-activated ion channels for remote control of neuronal firing. Nat Neurosci 7, 1381-1386 (2004)
- [27] M Volgraf, P Gorostiza, R Numano, R Kramer, E Isacoff and D Trauner: Allosteric control of an ionotropic gluatmate receptor with an optical switch. Nat Chem Biol 2, 47-52 (2006)
- [28] C Niswender and P Conn: Metabotropic glutamate receptors: physiology, pharmacology and disease. Annu Rev Pharmacol Toxicol 50, 295-322 (2010)
- [29] A Mourot, M Kienzler, M Banghart, T Fehrentz, F Huber, M Stein, R Kramer and D Trauner: Tuning photochromic ion channel blockers. ACS Chem Neurosci 2, 536-543 (2011)
- [30] B Gaub, M Berry, A Holt, A Reiner, M Kienzler, N Dolgova, S Nikonov, G Aguirre, W Beltran, J Flannery and EY Isacoff: Restoration of visual function by expression of a light-gated mammalian ion channel in retinal ganglion cells or ON-bipolar cells. Proc Natl Acad Sci U S A 111, E5574-5583 (2014)
- [31] A Rullo, A Reiner, A Reiter, D Trauner, E Isacoff and A Woolley: Long wavelength optical control of glutamate receptor ion channels using a tetra-ortho-substituted azobenzene derivative. Chem Comm 50, 14613-1461 (2014)
- [32] M Izquierdo-Serra, M Gascón-Moya, J Hirtz, S Pittolo, K Poskanzer, È Ferrer., Alibés, F Busqué, R Yuste, J Hernando and P Gorostiza: Two-photon neuronal and astrocytic stimulation with azobenzene-based photoswitches. J Am Chem Soc 136, 8693-8701 (2014)
- [33] I Tochitsky, A Polosukhina, V Degtyar, N Gallerani, C Smith, A Friedman, R Van Gelder, D Trauner, D Kaufer and R Kramer: Restoring visual function to blind mice with a photoswitch that exploits electrophysiological remodeling of retinal ganglion cells. Neuron 81, 800-813 (2014)
- [34] K Yau and R Hardie: Phototransduction motifs and variations. Cell 139, 246-264 (2009)
- [35] B Gaub, M Berry, A Holt, E Isacoff and J Flannery: Optogenetic vision restoration using rhodopsin for enhanced sensitivity. Mol Ther (2015), Epub ahead of print
- [36] Y Shichida and T Matsuyama: Evolution of opsins and phototransduction. Philos Trans R Soc B 364, 2881-2895 (2009)
- [37] H Bailes, L Zhuang and R Lucas: Reproducible and sustained regulation of Gαs signalling using a metazoan opsin as an optogenetic tool. PLoS One, 7, e30774 (2012)
- [38] O Masseck, K Spoida, D Dalkara, T Maejima, JM Rubelowski, L Wallhorn, E Deneris and S Herlitze: Vertebrate cone opsins enable sustained and highly sensitive rapid control of Gi/o signaling in anxiety circuitry. Neuron 81, 1263-1273 (2014)
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- [40] A Terakita, H Tsukamoto, M Koyanagi, M Sugahara, T Yamashita and Y Shichida: Expression and comparative characterization of Gq-coupled invertebrate visual pigments and melanopsin. J Neurochem 105, 883-890 (2008)
- [41] B Lin, A Koizumi, N Tanaka, S Panda and R Masland: Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc Natl Acad Sci U S A 105, 16009-16014 (2008)
- [42] Z Melyan, E Tarttelin, J Bellingham, R Lucas and M Hankins: Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433, 741-745 (2005)
- [43] T Tsunematsu, K Tanaka, A Yamanaka and A Koizumi: Ectopic expression of melanopsin in orexin/hypocretin neurons enables control of wakefulness of mice in vivo by blue light. Neurosci Res 75, 23-28 (2013)
- [44] J Nissilä, S Mänttäri, T Särkioja, H Tuominen, T Takala, M Timonen and S Saarela: Encephalopsin (OPN3) protein abundance in the adult mouse brain. J Comp Physiol A 198, 833-839 (2012)
- [45] D Kojima, S Mori, M Torii, A Wada, R Morishita and Y Fukada: UV-sensitive photoreceptor protein OPN5 in humans and mice. PLoS One 6, e26388 (2011)
- [46] M Koyanagi and A Terakita: Diversity of animal opsin-based pigments and their optogenetic potential. Biochim Biophys Acta 1837, 710-716 (2014)
- [47] E Oh, T Maejima, C Liu, E Deneris and S Herlitze: Substitution of 5-HT1A receptor signaling by a light-activated G protein-coupled receptor. J Biol Chem 285, 30825-30836 (2010)
- [48] K Spoida, O Masseck, E Deneris and S Herlitze: Gq/5-HT2c receptor signals activate a local GABAergic inhibitory feedback circuit to modulate serotonergic firing and anxiety in mice. Proc Natl Acad Sci U S A 111, 6479-6484 (2014)
- [49] M Audet and M Bouvier: Restructuring G-protein-coupled receptor activation. Cell 151, 14-23 (2012)
- [50] B Kobilka, T Kobilka, K Daniel, J Regan, M Caron and R Lefkowitz: Chimeric alpha 2-, beta 2-adrenergic receptors: delineation of domains involved in effector coupling and ligand binding specificity. Science 240, 1310-1316 (1988)
- [51] M Olah: Identification of A2a adenosine receptor domains involved in selective coupling to Gs. Analysis of chimeric A1/A2a adenosine receptors. J Biol Chem 272, 337-344 (1997)
- [52] S Verrall, M Ishii, M Chen, L Wang, T Tram and S Coughlin: The thrombin receptor second cytoplasmic loop confers coupling to Gq-like G proteins in chimeric receptors. Additional evidence for a common transmembrane signaling and G protein coupling mechanism in G protein-coupled receptors. J Biol Chem 272, 6898-6902 (1997)
- [53] L Kozell, CA Machida, RL Neve and KA Neve: Chimeric D1/D2 dopamine receptors. Distinct determinants of selective efficacy, potency, and signal transduction. J Biol Chem 269, 30299-30306 (1994)
- [54] S Wong, E Parker and E Ross: Chimeric muscarinic cholinergic: beta-adrenergic receptors that activate Gs in response to muscarinic agonists. J Biol Chem 265, 6219-6224 (1990)
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